Desiccation-Tolerant Plants in Dry Environments

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Desiccation-Tolerant Plants in Dry Environments Rev Environ Sci Biotechnol (2006) 5:269–279 DOI 10.1007/s11157-006-0015-y REVIEW PAPER Desiccation-tolerant plants in dry environments T.-N. Le Æ S. J. McQueen-Mason Received: 24 February 2006 / Accepted: 13 June 2006 / Published online: 14 July 2006 Ó Springer Science+Business Media B.V. 2006 Abstract The majority of terrestrial plants are wall-loosening activity during desiccation that unable to survive in very dry environments. enhances wall flexibility and promotes folding. However, a small group of plants, called ‘resur- rection’ plants, are extremely desiccation-tolerant Keywords Cell wall Æ Desiccation tolerance Æ and are capable of losing more than 90% of the Drought stress Æ Dry environments Æ Expansins Æ cellular water in vegetative tissues. Resurrection Resurrection plants Æ Water deficit plants can remain dried in an anabiotic state for several years and, upon rehydration, are able to resume normal growth and metabolism within Introduction 24 h. Vegetative desiccation tolerance is thought to have evolved independently several times Plants exhibit several strategies to deal with life in within the plant kingdom from mechanisms that extremely dry environments; namely avoidance, allow reproductive organs to survive air-dryness. resistance, or tolerance to desiccation (Levitt Resurrection plants synthesise a range of com- 1980). Some plants (e.g. annuals) complete their pounds, either constitutively or in response to life cycles during the part of the year when water dehydration, that protect various components of is plentiful and growth conditions are favourable, the cell wall from damage during desiccation and/ and avoid times during which desiccation is fre- or rehydration. These include sugars and late quent (e.g. summer). Desiccation avoidance may embryogenesis abundant (LEA) proteins that are enable plants to achieve maximal growth and thought to act as osmoprotectants, and free radi- productivity, but it also confines them to areas or cal-scavenging enzymes that limit the oxidative periods with favourable conditions. Other plants, damage during dehydration. Changes in the cell for example perennials such as cacti, have modi- wall composition during drying reduce the fied morphological structures that allow them to mechanical damage caused by the loss of water retain most of their cellular water and resist and the subsequent shrinking of the vacuole. equilibration with the air. These adaptations al- These include an increase in expansin or cell low desiccation-resistant plants to extend the range of conditions and habitats in which they can remain metabolically active throughout the year. & T.-N. Le ( ) Æ S. J. McQueen-Mason The main drawback for plants with a desiccation CNAP, Department of Biology, University of York, P.O. Box 373, York, YO10 5YW, UK survival strategy geared towards resistance is that e-mail: [email protected] growth often proceeds very slowly. A small group 123 270 Rev Environ Sci Biotechnol (2006) 5:269–279 of plants, the so-called ‘resurrection plants’ (Gaff factors), sugars and other compatible solutes in 1971), are extremely desiccation-tolerant, and can the protection and maintenance of cellular survive almost complete desiccation, usually integrity. We also review some adaptations of –1 considered as drying to < 0.1 g H2Og dry resurrection plants for surviving desiccation mass or to 10% absolute water content or less including changes in the cell wall and lipid com- (Alpert 2005). position, and the establishment of anti-oxidant Desiccation tolerance has been defined as the systems. ability of an organism to equilibrate its internal water potential with that of moderately dry air, and then resume normal function after rehydra- Evolution of desiccation tolerance tion (Alpert 2000). Air-dryness at a relative humidity of 50% at 28°C would equate to a water In order to colonize the land, the earliest terres- potential of – 100 MPa (Gaff 1997), a water trial plants must have been desiccation-tolerant at deficit that would be lethal to the majority of every stage of the life cycle (Oliver et al. 2005). modern day flowering plants. However, a few With the evolution of more complex vascular resurrection plants possess vegetative tissues that plants, desiccation tolerance was lost in vegetative can tolerate loss of greater than 90% of their tissues but was retained in reproductive tissues cellular water, and some can tolerate drying to (Oliver et al. 2000). The acquisition of desiccation water potentials as low as – 650 MPa without tolerance is part of a maturation program during injury (Gaff 1997). Resurrection plants are usu- normal seed development. The majority of ally found in habitats of sporadic rainfall, terrestrial plants today are capable of producing including rocky outcrops, and arid zones within desiccation-tolerant structures such as spores, tropical and subtropical areas (Rascio and La seeds and pollen which can remain viable in the Rocca 2005). It is estimated that there are about desiccated state for decades, or centuries, in the 300 angiosperms which possess vegetative desic- case of the ancient Nelumbo nucifera (sacred cation tolerance (Porembski and Barthlott 2000). lotus) seed from China (Shen-Miller et al. 1995). Desiccation-tolerant plants have been found in all The structural genes required for desiccation continents except Antarctica (Alpert 2000), and tolerance are not unique to resurrection plants, in all groups of seed plants except for the gym- but are also present in the genomes of desicca- nosperms (Oliver 1996). Resurrection plants, like tion-sensitive plants (Bartels and Salamini 2001). their desiccation-tolerant animal counterparts, However, resurrection plants may have enlisted are generally small in size. The absence of vege- genes normally expressed in seed tissue for tative desiccation tolerance within the gymno- expression in vegetative tissue to allow these sperms, or within any vascular plant more than plants to withstand desiccation (Illing et al. 2005). 3 m in height, is thought to be due to the physical For example, genes encoding late embryogenesis constraint of re-establishing water flow in the abundant (LEA) proteins (see below) that are xylem during rehydration after it has been inter- normally expressed in the seeds of desiccation- rupted during desiccation due to cavitation sensitive plants during embryo maturation (Close (Alpert 2005). 1996) have been isolated from drought-stressed This review will focus on the ability of vege- vegetative tissues of resurrection plants such as tative tissues of resurrection plants to survive Sporobolus stapfianus (Neale et al. 2000) and extreme desiccation. First we examine how des- Craterostigma plantagineum (Bartels 2005). iccation tolerance of vegetative tissues evolved in Recent phylogenetic evidence suggests that these vascular plants. Then we investigate the different vascular plants gained the ability to withstand mechanisms used by resurrection plants to protect desiccation of their vegetative tissues from a cell membranes and organelles during desicca- mechanism present first in spores, and that this tion, and to repair dehydration-induced damage evolution (or re-evolution) has occurred on at upon rehydration. This includes examining the least ten independent occasions within the roles of key proteins (e.g. LEAs and transcription angiosperms (Oliver et al. 2005). 123 Rev Environ Sci Biotechnol (2006) 5:269–279 271 Plant strategies to survive desiccation (Wood and Oliver 1999). Proteins whose synthe- sis is initiated or increased during rehydration Several different strategies are utilised by resur- after a desiccation event are termed rehydrins rection plants to survive desiccation. Some plants (Scott and Oliver 1994). A recent investigation of have evolved mechanisms that protect cellular a T. ruralis rehydration cDNA library has found membranes and organelles during desiccation. that many of the 10,368 expressed sequence tags Other plants employ a constitutive repair system (ESTs) encode gene products that are involved in which allows them to rapidly mobilize repair protein synthesis, ion and metabolite transport, mechanisms in the damaged cell upon rehydra- oxidative stress metabolism, and membrane tion. In general, both the protection and repair biosynthesis and repair (Oliver et al. 2004). mechanisms are used by resurrection plants, with Desiccation-tolerant angiosperms such as the mosses generally utilizing a repair mechanism and dicot C. plantagineum and the monocot S. stapfi- vascular plants using a protective mechanism anus utilise a protection-based strategy for sur- (Oliver 1996). Regardless of the strategy used by viving desiccation. These plants can persist in the a particular resurrection plant, three factors have air-dried state for months, and revive from the been identified as being crucial for surviving desiccated state even after several years. Desic- desiccation: maintaining life in the dried state, cation tolerance in C. plantagineum is induced in limiting the extent of damage to existing tissues so vegetative tissues upon slow drying of the whole that repair is unnecessary or manageable, and plant, and plants do not survive if dehydration mobilizing repair systems upon rehydration occurs too rapidly (Bartels and Salamini 2001). (Bewley 1979). Similarly, the desiccation-tolerant C. wilmsii also Tolerance to near-complete desiccation of exhibits substantial ultrastructural damage upon vegetative organs is a widespread capability in rapid drying (Cooper and Farrant 2002). This bryophytes (Rascio
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